Genome‐wide DNA methylation homeostasis influences jasmonate signaling and potato defenses against the potato tuber moth Phthorimaea operculella

BACKGROUND: DNA methylation is an epigenetic mechanism involved in plant defense, yet its role in insect resistance remains unclear. Although herbivory remodels plant methylomes, the links between DNA methylation, resistance traits, and phytohormone signaling remain unresolved. RESULTS: We induced genome-wide hypomethylation in potato plants, Solanum tuberosum L., using the DNA methyltransferase inhibitor 5-azacytidine (5-azaC), and assessed their resistance to the potato tuber moth (PTM), Phthorimaea operculella Zeller. Foliar application of 100 μm 5-azaC significantly reduced global DNA methylation in leaves and compromised resistance to Phthorimaea operculella. Larvae and adults displayed stronger feeding and oviposition preferences, respectively, for 5-azaC-treated plants and larvae gained 25.9% more weight on treated than on control plants. These dual defects were associated with marked decreases in trypsin proteinase inhibitor (TPI) accumulation and emission of the anti-herbivore volatiles such as β-caryophyllene. Moreover, hypomethylated plants had substantially lower levels of jasmonic acid (JA) and transcripts of JA biosynthetic genes. Exogenous methyl jasmonate (MeJA) restored resistance to Phthorimaea operculella by reinstating TPI accumulation and β-caryophyllene emission, whereas silencing of allene oxide cyclase gene (StAOC) caused opposite phenotype. Moreover, JA modulated genome-wide DNA methylation during herbivory and Phthorimaea operculella herbivory reduced promoter methylation of JA-related genes. CONCLUSION: Disrupting DNA methylation homeostasis compromises potato defenses and is associated with reduced JA-regulated defense outputs. Our findings reveal dynamic interplay between DNA methylation and JA-mediated herbivore defense in potato. © 2026 Society of Chemical Industry.